Francesco Tini

Giovanni Beccari

Hans J. L. Jørgensen

Frontiers in Plant Science

Directory of Open Access Journals

Frontiers in Plant ScienceOPEN ACCESSEDITED AND REVIEWED BYBrigitte Mauch-Mani,Université de Neuchâtel, Switzerland*CORRESPONDENCEFrancesco Tinifrancesco.tini@unipg.itRECEIVED 24 November 2023ACCEPTED 27 November 2023PUBLISHED 04 December 2023CITATIONBeccari G, Tini F and Jørgensen HJL (2023)Editorial: Current advances in themetabolism of mycotoxins in plants.Front. Plant Sci. 14:1343855.doi: 10.3389/fpls.2023.1343855COPYRIGHT© 2023 Beccari, Tini and Jørgensen. This isan open-access article distributed under theterms of the Creative Commons AttributionLicense (CC BY). The use, distribution orreproduction in other forums is permitted,provided the original author(s) and thecopyright owner(s) are credited and thatthe original publication in this journal iscited, in accordance with acceptedacademic practice. No use, distribution orreproduction is permitted which does notcomply with these terms.TYPE EditorialPUBLISHED 04 December 2023DOI 10.3389/fpls.2023.1343855Editorial: Current advancesin the metabolism ofmycotoxins in plantsGiovanni Beccari1, Francesco Tini1* and Hans J. L. Jørgensen21Department of Agricultural, Food and Environmental Sciences, University of Perugia, Perugia, Italy,2Department of Plant and Environmental Sciences, Faculty of Science, University of Copenhagen,Frederiksberg, DenmarkKEYWORDSsecondary metabolites, fungi, cereals, bean, Fusarium, Aspergillus, TrichodermaEditorial on the Research TopicCurrent advances in the metabolism of mycotoxins in plantsMycotoxins are toxic secondary metabolites (SM) produced by various genera offilamentous fungi. They can induce a wide variety of harmful effects in humans andanimals. Often, mycotoxin accumulation begins in plants when they are attacked bymycotoxigenic fungi. However, plants have the ability to transform and detoxify phytotoxicchemical compounds such as mycotoxins (Berthiller et al., 2007; Berthiller et al., 2013).Thus, plants can transform mycotoxins, and in some cases, the resulting compounds maybe harmless, while in others, they may be toxic, being considered as “masked mycotoxins”(Freire and Sant’Ana, 2018; Zhang et al., 2020). For some mycotoxins, the host’s ability tometabolize these compounds is well-known, while for others, limited data are available.Conversely, SM produced by non-pathogenic fungal microorganisms could have anantifungal role against pathogenic fungi (Rodrigo et al., 2022). SM can also interact withplant metabolism, enhancing the plant’s defence to counteract pathogens (Elhamoulyet al., 2022).For all these reasons, understanding the metabolism of mycotoxins in plants is a keyaspect of counterbalancing their spread in food/feed products and adopting mitigation tacticsto reduce human and animal health hazards. In this context, the objective of this ResearchTopic was to collect articles relative to the current advances in the metabolism of mycotoxins.This Research Topic contains five manuscripts that cover significant aspects of this field.The paper written by Meng et al. highlights introductory elements showing thepresence of mycotoxigenic fungi in cereal grain. They reported the presence ofAspergillus, Fusarium and Alternaria, as well as their abilities to produce mycotoxins, inwheat and paddy grains (fresh and stored samples) collected in 2021 from Shanghai(China). Fusarium sambucinum and species within Aspergillus section flavi were morefrequently found in paddy grains, whereas Alternaria was the predominant genus in wheat.Fusarium spp. were the main species in fresh grains and Aspergillus was predominant instored grains. In vitro assessments on potato dextrose agar demonstrated that Fusariumisolates were mainly capable of producing deoxynivalenol and zearalenone. Aflatoxins wereexclusively produced by Aspergillus section flavi. Alternaria species predominantlysynthesized alternariol, together with other mycotoxins like alternariol monomethylfrontiersin.org01Beccari et al. 10.3389/fpls.2023.1343855ether, altenuene, tenuazonic acid, tentoxin, and altenusin. Acombined analysis of the mycobiota and their mycotoxin-producing potential provides valuable insights into mycotoxin-production mechanisms, thereby facilitating the development ofeffective prevention and control strategies for wheat and paddy in aspecific geographic region.In addition to paddy and wheat grains, Aspergillus section flaviis also often associated with maize grains causing aflatoxinscontaminations (Smith et al., 2019). In this context, the paper byCastano-Duque et al. provides interesting discoveries on themodulation by flavonoids of aflatoxins accumulation fromAspergillus flavus in maize kernels. To understand the molecularmechanisms of maize resistance to A. flavus colonization andaflatoxin accumulation better, they performed a transcriptomicstudy in maize kernels infected by the fungus. They found asignificant association between flavonoid biosynthetic pathwaygenes and infection by A. flavus. This suggests that flavonoids cancontribute to host resistance mechanisms against aflatoxincontamination through the modulation of toxin accumulation inmaize kernels.Maize grains can also be colonized by other mycotoxigenicspecies such as those belonging to the genus Fusarium (Bryła et al.,2022). In this context, Cao et al. investigated the resistance of maizekernels to Fusarium ear rot (FER), caused by Fusariumverticillioides as well as fumonisin accumulation. For this,quantitative trait loci (QTLs) and bulk-segregant RNA-seqtechniques were utilized. Genetic regions within genetic bins 4.07-4.1, 6-6.01, 6.04-6.05, and 8.05-8.08 were linked to FER resistanceand reduced fumonisin levels. Transcriptome comparisons betweenresistant and susceptible inbred bulks at 10 days post-inoculationwith F. verticillioides identified 364 differentially expressed genes(DEGs). In resistant bulks, genes associated with fatty acid andstarch biosynthesis, cell division and phytosulfokine signalling weredownregulated. Conversely, genes tied to secondary metabolism,cell wall biosynthesis/rearrangement and flavonoid production wereupregulated, reflecting a growth-defence trade-off. Several DEGs,located within QTL confidence intervals and showing significantexpression differences between resistant and susceptible bulks, wereidentified as candidate genes for FER resistance andfumonisin reduction.Studying the same host-pathogen interaction, Cao et al.performed a metabolome study in maize, comparing recombinantinbred lines with and without inoculation with F. verticillioides. Themaize lines varied in resistance to the pathogen and the aim was toelucidate pathways involved in resistance and find markers for FERand fumonisin contamination in maize kernels. Data obtained 10days after inoculation explained differences between resistance andsusceptibility better than data from 3 days. It was found thatdifferences in membrane lipid homeostasis, methioninemetabolism and modulation of indolacetic acid conjugationappeared relevant when distinguishing between resistant andsusceptible lines. Furthermore, specific metabolites, such asFrontiers in Plant Science 02polyamine spermidine and the alkaloid isoquinoline appeared tobe interesting when looking for improvement of resistance to FERand reduction of fumonisin levels.SM produced by microorganisms may have an antifungal roleagainst phytopathogenic fungi. Among different microorganisms, thespecies of the genus Trichoderma are the most potent biocontrolagents in use today, among others because they produce a diverserange of antimicrobial SM (Khan et al., 2020). Cardoza et al. studiedthe biocontrol fungus Trichoderma arundinaceum, which has thepotential as a biological control agent, but also can producetrichothecene toxins. Three Trichoderma arundinaceum isolatesfrom bean fields produced trichothecene harzianum A (HA) andtrichodermol (an intermediate in the HA-biosynthesis). The threeisolates showed antifungal activity against the bean pathogensRhizoctonia solani and Sclerotinia sclerotiorum in vitro and this wasascribed to HA production. Furthermore, seed treatment with theTrichoderma-isolates gave faster germination and, in some cases,increased growth of aerial parts of bean plants. Transcriptomics ofbean plants inoculated with the T. arundinaceum isolates indicatedthat HA production increased the expression of plant defence-relatedgenes, especially chitinase-encoding genes. Collectively, the studyindicated that Trichoderma species can induce resistance in plantswithout negative effects on plant growth.The collection of articles on this Research Topic providesinteresting information on the presence of mycotoxins in plants,the plant’s activity to reduce the accumulation of mycotoxins, aswell as the interaction of some SM with the host, enhancing itsability to counteract pathogens.Author contributionsGB: Conceptualization, Writing – original draft, Writing –review & editing. FT: Conceptualization, Writing – original draft,Writing – review & editing. HJ: Conceptualization, Writing –original draft, Writing – review & editing.AcknowledgmentsThe editors would like to thank all editors and reviewers whoevaluated manuscripts of this Research Topic.Conflict of interestThe authors declare that the research was conducted in theabsence of any commercial or financial relationships that could beconstrued as a potential conflict of interest.The author(s) declared that they were an editorial boardmember of Frontiers, at the time of submission. This had noimpact on the peer review process and the final decisionfrontiersin.orgBeccari et al. 10.3389/fpls.2023.1343855Publisher’s noteAll claims expressed in this article are solely those of the authorsand do not necessarily represent those of their affiliatedFrontiers in Plant Science 03organizations, or those of the publisher, the editors and thereviewers. Any product that may be evaluated in this article, orclaim that may be made by its manufacturer, is not guaranteed orendorsed by the publisher.ReferencesBerthiller, F., Crews, C., Dall’Asta, C., De Saeger, S., Haesaert, G., Karlovsky, P., et al. (2013).Maskedmycotoxins: a review.Mol. Nutr. Food Res. 57, 165–186. doi: 10.1002/mnfr.201100764Berthiller, F., Lemmens, M., Werner, U., Krska, R., Hauser, M. T., Adam, G., et al.(2007). Short review: metabolism of the Fusarium mycotoxins deoxynivalenol andzearalenone in plants. Mycotoxin Res. 23, 68–72. doi: 10.1007/BF02946028Bryła, M., Pierzgalski, A., Zapaśnik, A., Uwineza, P. A., Ksieniewicz-Woźniak, E.,Modrzewska, M., et al. (2022). Recent research on fusarium mycotoxins in maize—Areview. Foods 11, 3465. doi: 10.3390/foods11213465Elhamouly, N. A., Hewedy, O. A., Zaitoon, A., Miraples, A., Elshorbagy, O. T., Hussien,S., et al. (2022). The hidden power of secondary metabolites in plant-fungi interactionsand sustainable phytoremediation. Front. Plant Sci. 13. doi: 10.3389/fpls.2022.1044896Freire, L., and Sant’Ana, A. (2018). Modified mycotoxins: an updated review on theirformation, detection, occurrence, and toxic effects. Food Chem. Toxicol. 111, 189–205.doi: 10.1016/j.fct.2017.11.021Khan, R. A. A., Najeeb, S., Hussain, S., Xie, B., and Li, Y. (2020). Bioactive secondarymetabolites from Trichoderma spp. against phytopathogenic fungi. Microorganisms 8,817. doi: 10.3390/microorganisms8060817Rodrigo, S., Garcıá-Latorre, C., and Santamaria, O. (2022). Metabolites produced byfungi against fungal phytopathogens: review, implementation and perspectives. Plants11, 81. doi: 10.3390/plants11010081Smith, J. S., Williams, W. P., andWindham, G. L. (2019). Aflatoxin in maize: a reviewof the early literature from “moldy-corn toxicosis”. to Genet. aflatoxin accumulationresistance Mycotoxin Res. 35, 11–128. doi: 10.1007/s12550-018-00340-wZhang, Z., Nie, D., Fan, K., Yang, J., Guo, W., Meng, J., et al. (2020). A systematicreview of plant-conjugated masked mycotoxins: occurrence, toxicology, andmetabolism. Crit . Rev. Food Sci . Nutr. 60, 1523–1537. doi : 10.1080/10408398.2019.1578944frontiersin.org

Editorial: Current advances in the metabolism of mycotoxins in plants

https://www.frontiersin.org/articles/10.3389/fpls.2023.1343855/pdf?isPublishedV2=False

Editorial: Current advances in the metabolism of mycotoxins in plants

Abstract

Similar works

Full text

Available Versions

Directory of Open Access Journals